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A Pattern of Unique Embryogenesis Occurring Via Apomixis in Carya Cathayensis

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A Pattern of Unique Embryogenesis Occurring Via Apomixis in Carya Cathayensis BIOLOGIA PLANTARUM 56 (4): 620-627, 2012 DOI: 10.1007/s10535-012-0256-2 A pattern of unique embryogenesis occurring via apomixis in Carya cathayensis B. ZHANG1,2a, Z.J. WANG1a, S.H. JIN1a, G.H. XIA1, Y.J. HUANG1 and J.Q. HUANG1* School of Forestry and Biotechnology, Zhejiang A & F University, Lin’an 311300, P.R. China1 Bureau of Agricultural Economics of Haiyan, Haiyan 314300, P.R. China2 Abstract Apomixis represents an alteration of classical sexual plant reproduction to produce seeds that have essentially clonal embryos. In this report, hickory (Carya cathayensis Sarg.), which is an important oil tree, is identified as a new apomictic species. The ovary has a chamber containing one ovule that is unitegmic and orthotropous. Embryological investigations indicated that the developmental pattern of embryo sac formation is typical polygonum-type. Zygote embryos were not found during numerous histological investigations, and the embryo originated from nucellar cells. Nucellar embryo initials were found both at the micropylar and chalazal ends of the embryo sac, but the mature embryo developed only at the nucellar beak region. The mass of the nucellar embryo initial at the nucellar beak region developed into a nucellar embryo or split into two nucellar proembryos. The later development of the nucellar embryo was similar to the zygotic embryo and progressed from globular embryo to heart-shape embryo and to cotyledon embryo. Additional key words: adventitious embryony, female gametophyte, hickory, nucellar embryo. Introduction The term apomixis was first introduced by Winkler 3) two gametophytic types diplospory and apospory (1908) to refer to the “substitution of sexual reproduction (Peggy 2006, Koltunow 1993). Adventitious embryos can by an asexual multiplication process without nucleus and arise from two different tissues of the mature ovule, cell fusion”. Apomixis in flowering plants is the asexual namely the nucellus and the inner integument formation of seed directly from the maternal tissues of the (Lakshmanan and Ambegaokar 1984, Miles 2007). The ovule, avoiding meiosis and fertilization (Bicknell and form of the nucellus is common and this has been Koltunow 2004). Seeds resulting from apomixis are described in detail in Citrus, which is a model system for genetically identical to maternal plants, which is studying nucellar embryony. important for promoting the breeding process through Hickory (Carya cathayensis Sarg.), a member of the fixing hybrid vigor and arousing researchers’ interest family Juglandaceae, is an important oil tree of high (Hanna 1995, Koltunow et al. 1995a, Savidan 2000). economic value (Li 2003). In walnut, apomixis was Apomixis has been described in more than 400 flowering confirmed (Loiko 1990, Asadian and Pieber 2005), and plant species belonging to over 40 families (Carman later it was investigated in different cultivars using 1997). Among fruit tree species, only a few show this isoenzyme analysis (San and Dumanoğlu 2006, Wu et al. phenomenon and these fruits generally propagate 2006). The mechanisms of apomixis in walnut have been vegetatively, including citrus and mango (Mo et al. 2005). reported as adventitious embryony (Valdiviesso 1990), Apomixis can be divided broadly into three types: apospory (Terziiski and Stefanova 1990) or diplospory 1) adventitious embryony, 2) a sporophytic type, or (Sartorius and Stosser 1991). Sartorius and Stösser (1997) ⎯⎯⎯⎯ Received 7 April 2011, accepted 7 October 2011. Abbreviations: AFLP - amplified fragment length polymorphism; DAP - days after pollination; FCSS - flow cytometric seed screening; SSR - simple sequence repeat. Acknowledgments: This study was supported by the National Natural Science Foundation of China (30872047, 31170584 and 31100229), the Zhejiang Provincial Natural Science Foundation (z307534 and Y3110311). a - These authors contributed equally to this work. * Corresponding author; fax: (+86) 571 63740809, e-mail: [email protected] 620 HICKORY IS A NEW APOMICTIC SPECIES and Chen et al. (2000) reported development of apomictic differences between the hybrids and parents were embryos from the egg cell in different walnut cultivars. analyzed. Differential bands were found between the Schanderl (1964) reported that the development of paternal and maternal parents, as well as between the apomictic embryos in walnut was diplosporic and not by paternal parent and the progeny, but there was no nucellar embryony. During our previous study with difference between the maternal parent and the progeny hickory (Wang et al. 2010), we observed a certain or amongst the progeny (Wang et al. 2010). In addition, proportion of polyembryonic seedlings (9.04 %). flower bud differentiation in hickory was studied in detail Furthermore, we conducted a hybrid experiment between (Huang et al. 2006, 2007). The aim of the present study hickory and pecan (C. illinoensis). The hybrids showed was to investigate the female gametophyte and embryo variations in fruit shape, pericarp colour and seed size development in hickory to understand the mechanisms of and mass. Using short-sequence repeat (SSR) and its reproductive processes. amplified fragment length polymorphism (AFLP), Materials and methods A 50-year-old adult hickory (Carya cathayensis Sarg.) August. All the collected materials were fixed and stored tree from Lin’an city, Zhejiang province (China) was in FAA (70 % ethanol + glacial acetic acid + form- chosen as the mother tree. The female flowers were aldehyde; 90:5:5). Fruits grew rapidly until mid-June. bagged when the stigma began to turn red on 11 May Thus, the shells of any large fruits that were collected 2010. During the pollination period, the female flowers were removed or the ovules were directly isolated before were pollinated with mixed pollen from the mother tree fixing. Pistils and ovules were dehydrated in an ascending and surrounding trees on 17 May. One week later the series of ethanol, cleared in xylene and embedded in paper bags were removed once male inflorescences had paraffin. After trimming, paraffin blocks of tissue were faded. cut into 7 - 8 µm slices using a microtome (Leica When florets were visible (approximately 10 mm), RM2235, Leica Microsystems, Germany). Dry sections male flowers were collected every 4 d, and female were stained with safranin-fast green and iron flowers were collected at different developmental stages hematoxylin (Gao et al. 2010, Lin et al. 2010). according to the colour of the stigma. After pollination, Observations were carried out with a microscope female flowers and young fruits were collected every day (Olympus BX 60, Tokyo, Japan) and photographs were during the first 7 d, and then at 4-d intervals until mid- taken with the auto-photo system. Results Hickory is a monoecious tree with male flowers that are The ovary had a chamber containing one ovule that ternate aments and female flowers that form a terminal was unitegmic and orthotropous (Fig. 2A). In late April, spike of 3 - 4 florets. The floret is naked and without the ovule primordium was initiated in the mid-region of perianth. At the end of April, the floret was coated by the ovary, and then the integument primordium began to four bracts, which could be seen easily with the naked develop. The ovules had no funiculus and single eye (Fig. 1B). Afterwards, the bracts unfolded gradually integument. However, this integument did not completely with the development of the florets. During early May, cover the micropylar end of the nucellus and the the stigma appeared and then green circular spots were micropyle. Indeed, integument length was approximately presented (Fig. 1C). The pistil developed and extended half the length of the ovule during the mature embryo sac outwards and, due to the different growth rate of the pistil stage (Fig. 2B). tissues, it presented a dark-green rhombus after 2 - 3 d In early May, the megaspore mother cell, which was (Fig. 1D). The stigma colour changed from light red to different from surrounding nucellar cells, formed in the bright red to purplish red during the developmental stages middle of the nucellus. At this stage, stigmas of florets (Figs. 1E, 2H), and after it was pollinated, it quickly turned red starting from the central parts. Compared with turned dark (Fig. 1H). From mid-May to the mid-June the nucellar cells, the megaspore mother cell had a larger fruit size increased from 2.41 ± 0.07 mm on May 18 to nucleus and denser cytoplasm (Fig. 2C). Dyad (Fig. 2D) 9.24± 0.08 mm on June 24 and the average growth rate and tetrad formed after megasporocyte meiosis. At the was 0.18 mm per day. From June 24 to August 12, the tetrad stage, four megaspores aligned linearly along the fruits enlarged greatly and mean diameter increased to plane from micropylar to chalazal ends (Figs. 2E,F). 30.3 ± 0.12 mm. After that, the fruit diameter did not Then, the megaspore at the chalazal end became a increase up to harvest in early September (Figs. 1I,O). functional megaspore, while the others did not develop 621 B. ZHANG et al. Fig. 1. Morphological observations of floret and fruit development. A - Female flower bud begins to differentiate at the apical end of the spring shoot at 17 April, bar = 0.5 mm. B - Florets coated with bracts become macroscopic by 4 May, bar = 1 mm. C - Female flower with three florets which are coated with four bracts at 9 May, bar = 6 mm. D - Naked florets with no perianth and rhombus- shape stigma which is not coated in bracts at 11 May, bar = 4 mm. E - Florets with light red stigmas at 13 May, bar = 5 mm. F - Florets with bright red stigmas at 16 May, bar = 4 mm. G - Florets with purplish red stigmas at 18 May, bar = 4 mm. H -Florets with dark purple stigmas at 5 DAP, bar = 5 mm. I - Young fruits at 10 DAP, bar = 2 mm. J - Young fruits at 26 DAP, bar = 3 mm. K - Young fruits at 30 DAP, bar = 3 mm.
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